Phylogeographic analysis of shrubby beardtongues reveals range expansions during the Last Glacial Maximum and implicates the Klamath Mountains as a hotspot for hybridization

Abstract

Quaternary glacial cycles often altered species’ geographic distributions, which in turn altered the geographic structure of a species’ genetic diversity. In many cases, glacial expansion forced species in temperate climates to contract their ranges and reside in small pockets of suitable habitat (refugia), where they were likely to interact closely with other species, setting the stage for potential gene exchange. These introgression events, in turn, would have degraded species boundaries, making the inference of phylogenetic relationships challenging. Using high-throughput sequence data, we employ a combination of species distribution models, models of demographic history, and hybridization tests to assess the effect of glaciation on the geographic distributions, phylogenetic relationships, and patterns of gene flow of five species of Penstemon subgenus Dasanthera, long-lived shrubby angiosperms distributed throughout the Pacific Northwest of North America. Surprisingly, we find that rather than reducing their ranges to small refugia, most Penstemon subgenus Dasanthera species experienced increases in suitable habitat during the Last Glacial Maximum. We also find substantial evidence for gene exchange between species, with the bulk of introgression events occurring in or near the Klamath Mountains of southwestern Oregon and northwestern California. Subsequently, our phylogenetic inference reveals blurred taxonomic boundaries in the Klamath Mountains, where introgression is most prevalent. Our results question the classical paradigm of temperate species’ responses to glaciation, and highlight the importance of contextualizing phylogenetic inference with the demographic histories of the species of interest.

Phylogeographic analysis of shrubby beardtongues reveals range expansions during the Last Glacial Maximum and implicates the Klamath Mountains as a hotspot for hybridization

“…All processed sequence reads, scripts, and output files for analyses conducted in this manuscript have been made available on Dryad (Stone & Wolfe, 2021; https://doi.org/10.5061/dryad. n5tb2 rbtf).…”

The past, present, and future of ecogeographic isolation between closely related Aquilegia plants

“…For example, average temperatures in the LGM were substantially colder than they are today, and became increasingly hot after the LGM, reaching a temperature peak near the MID (Otto-Bliesner et al, 2006;Renssen et al, 2009;Wanner et al, 2008). The dramatic fluctuations in climate had a significant impact on species distributions, resulting in fragmented habitats among populations or more overlapping in species ranges between relatives (Hewitt, 1999;Stone & Wolfe, 2021). So we expected that the strength of the ecogeographic barrier between related species could be dynamic and change over time as a consequence of climate changes.…”

“…Unlike the classical paradigm of temperate species' responses to glaciation, we found that only one species, A. rockii, contracted its ranges to small pockets of suitable habitat, while the other three species experienced an increase in suitable habitat during the LGM relative to the present day. A recent study on Penstemon species in the Pacific Northwest of North America also experienced increased suitable habitat during the GLM, resulting in gene exchange between species (Stone & Wolfe, 2021).…”